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Casewell Phd 2010 Bangor University DOCTOR OF PHILOSOPHY The Genetic Basis of Venom Variation in the Genus Echis: Causes, Correlates and Consequences Casewell, Nicholas Award date: 2010 Awarding institution: Bangor University Link to publication General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. • Users may download and print one copy of any publication from the public portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying the publication in the public portal ? Take down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Download date: 05. Oct. 2021 PRI F Y S G O L BANGOR UNIVERSITY The Genetic Basis of Venom Variation in the Genus Echis: Causes, Correlates and Consequences Nicholas Robert Casewell Supervisors: Wolfgang Wiister and Robert Harrison Thesis to be submitted for the degree of Doctor of Philosophy at Bangor University Molecular Ecology and Evolution of Reptiles Unit School of Biological Sciences Bangor University March 31,2010 SIGNED DECLARATION FORM NOT TO BE INCLUDED IN THE DIGITISED THESIS Ill ABSTRACT Variation in venom components is inherent to multiple taxonomical levels of the Serpentes and can impact significantly upon the symptomatology of envenoming and the efficacy of antivenoms. Snake venom composition is thought to be subject to strong natural selection as a result of adaptations to specific diets, although no direct link at the molecular level has elucidated the evolutionary adaptations responsible for driving the optimisation of venom components to specific prey items. Venom gland cDNA libraries were constructed for three species of the genus Echis (E. pyramidum leakeyi, E. coloratus and E. carinatus sochureki) to complement the existing E. ocellatus transcriptome. Generated expressed sequence tags were clustered with a modified CLOBB algorithm, which was demonstrated to confer increases in the integrity of cluster formation and membership over the standard CLOBB2 algorithm. Comparative analyses of multiple Echis venom gland transcriptomes revealed the presence of snake venom metalloproteinases (SVMP), C-type lectins, phopholipases A2, serine proteases (SP), L-amino oxidases and growth factors throughout the genus. Putative novel venom proteins exhibiting similarity to lysosomal acid lipase/cholesteryl ester hydrolase and the metallopeptidases dipeptidyl peptidase III and neprilysin were also identified in the venom glands of individual species. Phylogenetic and gene tree parsimony analyses provide the first evidence of the genomic basis of snake venom adaptations as a response to alterations in diet, with SVMP and SP toxin families exhibiting diet- associated gene events that correlate strongly with a dietary shift to vertebrate feeding in E. coloratus. The diversification and retention of these coagulopathic and haemorrhagic toxins in E. coloratus correlates with significant differences in venom function in the form of in vivo haemorrhage, providing genetic and functional evidence of coevolution between diet and venom components. Selective evolutionary pressures were also determined to be capable of confounding the derivation of species relationships from toxin data, suggesting venom components should not be used as primary species identifiers. Finally, the E. ocellatus antivenom EchiTabG® was demonstrated to effectively neutralise the venom of African members of the genus Echis in spite of considerable intra-generic variation in venom components. These results strongly advocate the geographical expansion of EchiTabG® to treat Echis envenomations throughout the African continent. IV ACKNOWLEDGEMENTS First and foremost I would like to thank my supervisor Wolfgang Wüster for all of his help and guidance over the past three years. His enthusiasm, assistance and engagement of my ideas have been integral for my progression as a scientist and the resulting thesis you are reading today; for this I will always be grateful. I must also thank Wolfgang for the design of the project, which has provided a fantastic framework for the exploration of snake venom evolution and other aspects of biology that have fascinated me. I would also like to thank my co-supervisors at the Alistair Reid Venom Research Unit at the Liverpool School of Tropical Medicine. Rob Harrison has provided invaluable advice on all aspects of this project and has had a significant impact upon my personal development as a scientist. I thank him also for encouraging me to delve into the immunological aspect of venoms; the skills I have developed subsequently are the result of his guidance. Simon Wagstaff has been hugely supportive throughout the past three years and has successfully guided me through the murky world of cDNA and sequence bioinformatics. He has always been there to provide guidance, especially with the (occasionally stupid) questions I need answering. I must also thank MicroPharm Ltd and their staff for their sponsorship as a NERC PhD CASE partner. I thank John Landon and Ibrahim Al-Abdulla particularly for taking their time to show me how antivenoms are made, as well as raising antibodies and providing antivenom for my own research studies. General thanks go to Paul Rowley for his expert herpetological assistance, Damien Egan and Paul Vercammen (Breeding Centre for Endangered Arabian Wildlife, United Arab Emirates) for providing specimens of E. c. sochureki, Jean-François Trape and Youssouph Mané (Institut de Recherche pour le Développement, Dakar) for fieldwork assistance, Ann Hedley and Mark Blaxter (NERC Molecular Genetics Facility, University of Edinburgh) for providing sequencing and bioinformatic advice regarding the PartiGene pipeline, Tim Booth, Bela Tiwari and Jorge Soares (NERC Environmental Bioinformatics Centre, Oxford) for general bioinformatic advice, Michael Berenbrink (School of Biological Sciences, University of Liverpool) V for assistance with SigmaPlot and Wayne Maddison (University of British Columbia, Canada) for help with Mesquite. Big thanks go to Cath, Axel, Yvonne, Darren, Rachel and Camila for being great office mates, making me laugh and helping me through the more stressful times! My family have always encouraged me to follow a career path that I am passionate about and they have provided every support possible during the past twenty-five years. I am eternally grateful for everything they have done for me and without them I would not be in this position today. I look forward to many more conversations where I attempt to explain what I have been doing for the past three years! Finally, I thank my wife Lisa, who has been by my side supporting my decisions for a lot longer than the past three years. I am grateful for the sacrifices she made in her career so that I may undertake this PhD and for always being there through the good and bad times. I can only apologise to her for my numerous stresses about work- related issues, but she has always responded with humour and a positive attitude that makes things better. Thanks for the tea and biscuits and thank you so much for everything else. VI PREFACE Chapter 1 describes introductory information on the nature of venoms, their evolution and the genus Echis, whilst Chapter 2 details the methods utilised to generate DNA sequence information from venom glands. The experimental chapters (Chapters 3-7) are presented in the form of publication papers and therefore contain detailed methodological sections outlining the specific methods utilised for each chapter of experimental work. All experimental work has been undertaken by myself except where otherwise specified at the end of an experimental chapter. Chapter 8 discusses and summarises the conclusions drawn from the experimental chapters. Chapter 3 outlines a comparative study between differing bioinformatic algorithms that cluster expressed sequence tags (ESTs). The results strongly support the use of a modified CLOBB algorithm as the optimal method for clustering snake venom gland derived ESTs. Chapter 4 presents comparative results of four sequenced Echis venom gland cDNA libraries in the form of transcriptomic profiles. Substantial intra-generic variation in the representation of toxin components was observed and three novel putative venom components are described. This chapter has been published in the journal BMC Genomics - the published manuscript is presented in Appendix VI. Chapter 5 investigates the selective influence of diet on the evolution of venom components in the genus Echis. Gene tree parsimony analyses provide evidence of multiple toxin families exhibiting diet-associated gene events that correlate with a reversion to vertebrate-feeding. This chapter has been submitted for publication to the journal Proceedings of the National Academy of Sciences, USA and is pending reviewer and editorial decisions. Chapter 6 assesses the value of venom-derived toxin family gene trees as species tree predictors. Gene tree parsimony of multiple toxin trees largely failed to infer species trees congruent with each other or robustly supported phylogenies. This chapter has been invited for resubmission for publication
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